Allopolyploidy: An Underestimated Driver in Juniperus Evolution

. 2023 Jun 30 ; 13 (7) : . [epub] 20230630

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37511854

Allopolyploidy is considered as a principal driver that shaped angiosperms' evolution in terms of diversification and speciation. Despite the unexpected high frequency of polyploidy that was recently discovered in the coniferous genus Juniperus, little is known about the origin of these polyploid taxa. Here, we conducted the first study devoted to deciphering the origin of the only hexaploid taxon in Juniperus along with four of its closely related tetraploid taxa using AFLP markers with four primers combinations. Phylogenetic analysis revealed that the 10 studied species belong to 2 major clusters. J. foetidissima appeared to be more related to J. thurifera, J. sabina, and J. chinensis. The Bayesian clustering analysis showing a slight variation in genetic admixture between the studied populations of J. foetidissima, suggesting an allopolyploid origin of this species involving J. thurifera and J. sabina lineages, although a purely autopolyploidy origin of both J. thurifera and J. foetidissima cannot be ruled out. The admixed genetic pattern revealed for J. seravschanica showed that the tetraploid cytotypes of this species originated from allopolyploidy, whereas no clear evidence of hybridization in the origin of the tetraploid J. thurifera and J. chinensis was detected. This study provides first insights into the polyploidy origin of the Sabina section and highlights the potential implication of allopolyploidy in the evolution of the genus Juniperus. Further analyses are needed for a more in-depth understanding of the evolutionary scenarios that produced the observed genetic patterns.

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Alix K., Gérard P.R., Schwarzacher T., Heslop-Harrison J.S. Polyploidy and interspecific hybridization: Partners for adaptation, speciation and evolution in plants. Ann. Bot. 2017;120:183–194. doi: 10.1093/aob/mcx079. PubMed DOI PMC

Mallet J. Hybrid Speciation. Nature. 2007;446:279–283. doi: 10.1038/nature05706. PubMed DOI

Paun O., Forest F., Fay M.F., Chase M.W. Hybrid speciation in angiosperms: Parental divergence drives ploidy. New Phytol. 2009;182:507–518. doi: 10.1111/j.1469-8137.2009.02767.x. PubMed DOI PMC

Soltis P.S., Soltis D.E. The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 2009;60:561–588. doi: 10.1146/annurev.arplant.043008.092039. PubMed DOI

Wu H., Ma Z., Wang M.M., Qin A.L., Ran J.H., Wang X.Q. A high frequency of allopolyploid speciation in the gymnospermous genus Ephedra and its possible association with some biological and ecological features. Mol. Ecol. 2016;25:1192–1210. doi: 10.1111/mec.13538. PubMed DOI PMC

Wu H., Yu Q., Ran J.H., Wang X.Q. Unbiased subgenome evolution in allotetraploid species of Ephedra and its implications for the evolution of large genomes in gymnosperms. Genome Biol. Evol. 2021;13:evaa236. doi: 10.1093/gbe/evaa236. PubMed DOI PMC

Farhat P., Hidalgo O., Robert T., Siljak-Yakovlev S., Leitch I.J., Adams R.P., Bou Dagher-Kharrat M. Polyploidy in the conifer genus Juniperus: An unexpectedly high rate. Front. Plant Sci. 2019;10:676. doi: 10.3389/fpls.2019.00676. PubMed DOI PMC

Adams R.P. Junipers of the World: The Genus Juniperus. 4th ed. Trafford Publishing Co; Bloomington, IN, USA: 2014.

Nagano K., Matoba H., Yonemura K., Matsuda Y., Murata T., Hoshi Y. Karyotype analysis of three Juniperus species using Fluorescence in Situ Hybridization (FISH) with two ribosomal RNA genes. Cytologia. 2007;72:37–42. doi: 10.1508/cytologia.72.37. DOI

Romo A., Hidalgo O., Boratyński A., Sobierajska K., Jasińska A.K., Vallès J., Garnatje T. Genome size and ploidy levels in highly fragmented habitats: The case of western mediterranean Juniperus (Cupressaceae) with special emphasis on J. thurifera L. Tree Genet. Genomes. 2013;9:587–599. doi: 10.1007/s11295-012-0581-9. DOI

Vallès J., Garnatje T., Robin O., Siljak-Yakovlev S. Molecular cytogenetic studies in western Mediterranean Juniperus (Cupressaceae): A constant model of GC-rich chromosomal regions and rDNA loci with evidences for paleopolyploidy. Tree Genet. Genomes. 2015;11:43. doi: 10.1007/s11295-015-0860-3. DOI

Farhat P., Siljak-Yakovlev S., Adams R.P., Bou Dagher Kharrat M., Robert T. Genome size variation and polyploidy in the geographical range of Juniperus sabina L. (Cupressaceae) Bot. Lett. 2019;166:134–143. doi: 10.1080/23818107.2019.1613262. DOI

Bou Dagher-Kharrat M., Abdel-Samad N., Douaihy B., Bourge M., Fridlender A., Siljak-Yakovlev S., Brown S.C. Nuclear DNA C-Values for Biodiversity Screening: Case of the Lebanese Flora. Plant Biosyst. Int. J. Deal. Asp. Plant Biol. 2013;147:1228–1237. doi: 10.1080/11263504.2013.861530. DOI

Hirayoshi I., Nakamura Y. Chromosome number of Sequoia sempervirens. Bot. Zool. 1943;11:73–75.

Mouterde P. Nouvelle Flore du Liban et de La Syrie. Editions de l’Impr. Catholique; Beyrouth, Lebanon: 1966.

Meudt H.M., Clarke A.C. Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci. 2007;12:106–117. doi: 10.1016/j.tplants.2007.02.001. PubMed DOI

Kokotovic B., Friis N.F., Jensen J.S., Ahrens P. Amplified-Fragment Length Polymorphism Fingerprinting of Mycoplasma species. J. Clin. Microbiol. 1999;37:3300–3307. doi: 10.1128/JCM.37.10.3300-3307.1999. PubMed DOI PMC

Bou Dagher-Kharrat M., Mariette S., Lefèvre F., Fady B., Grenier-de March G., Plomion C., Savouré A. Geographical diversity and genetic relationships among Cedrus species estimated by AFLP. Tree Genet. Genomes. 2007;3:275–285. doi: 10.1007/s11295-006-0065-x. DOI

Jacobs M.M., van den Berg R.G., Vleeshouwers V.G., Visser M., Mank R., Sengers M., Hoekstra R., Vosman B. AFLP analysis reveals a lack of phylogenetic structure within Solanum section Petota. BMC Evol. Biol. 2008;8:145. doi: 10.1186/1471-2148-8-145. PubMed DOI PMC

Dasmahapatra K.K., Hoffman J.I., Amos W. Pinniped phylogenetic relationships inferred using AFLP markers. Heredity. 2009;103:168–177. doi: 10.1038/hdy.2009.25. PubMed DOI

Prebble J., Meudt H., Garnock-Jones P. Phylogenetic relationships and species delimitation of New Zealand Bluebells (Wahlenbergia, Campanulaceae) based on analyses of AFLP data. N. Z. J. Bot. 2012;50:365–378. doi: 10.1080/0028825X.2012.698624. DOI

Adams R.P., Farhat P., Shuka L., Siljak-Yakovlev S. Discovery of Juniperus sabina var. balkanensis R. P. Adams and A. N. Tashev in Albania and relictual polymorphisms found in nrDNA. Phytologia. 2018;100:187–194.

Farhat P., Takvorian N., Avramidou M., Garraud L., Adams R.P., Siljak-Yakovlev S., Bou Dagher-Kharrat M., Robert T. First evidence for allotriploid hybrids between Juniperus thurifera and J. sabina in a sympatric area in the French Alps. Ann. For. Sci. 2020;77:93. doi: 10.1007/s13595-020-00969-7. DOI

Farhat P., Siljak-Yakovlev S., Valentin N., Fabregat C., Lopez-Udias S., Salazar-Mendias C., Altarejos J., Adams R.P. Gene flow between diploid and tetraploid junipers—Two contrasting evolutionary pathways in two Juniperus populations. BMC Evol. Biol. 2020;20:148. doi: 10.1186/s12862-020-01688-3. PubMed DOI PMC

Douaihy B.C. Ph.D. Thesis. Préparée en co-tutelle entre la Faculté des sciences de l’Université Saint-Joseph de Beyrouth et Museum National D’Histoire Naturelle; Paris, France: 2011. Caractérisation Écogéographique et Génétique de Juniperius excelsa Dans l’est Du Bassin Méditerranée.

Doyle J.J., Doyle J.L. Isolation of plant DNA from fresh tissue. Focus. 1990;12:39–40.

Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Friters A., Pot J., Paleman J., Kuiper M., et al. AFLP: A New Technique for DNA Fingerprinting. Nucleic Acids Res. 1995;23:4407–4414. doi: 10.1093/nar/23.21.4407. PubMed DOI PMC

Bonin A., Bellemain E., Bronken Eidesen P., Pompanon F., Brochmann C., Taberlet P. How to track and assess genotyping errors in population genetics studies: Tracking and assessing genotyping errors. Mol. Ecol. 2004;13:3261–3273. doi: 10.1111/j.1365-294X.2004.02346.x. PubMed DOI

Vekemans X., Beauwens T., Lemaire M., Roldan-Ruiz I. Data from Amplified Fragment Length Polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol. Ecol. 2002;11:139–151. doi: 10.1046/j.0962-1083.2001.01415.x. PubMed DOI

Nei M., Li W.H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA. 1979;76:5269–5273. doi: 10.1073/pnas.76.10.5269. PubMed DOI PMC

Letunic I., Bork P. Interactive Tree Of Life (ITOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:293–296. doi: 10.1093/nar/gkab301. PubMed DOI PMC

Adams R.P., Schwarzbach A.E., Tashev A.N. Chloroplast capture by a new variety, Juniperus sabina var. balkanensis R. P. Adams and A. N. Tashev, from the Balkan Peninsula: A putative stabilized relictual hybrid between J. sabina and ancestral J. thurifera. Phytologia. 2016;98:100–111.

Adams R.P., Boratynski A., Marcysiak K., Roma-Marzio F., Peruzzi L., Bartolucci F., Conti F., Mataraci T., Schwarzbach A.E., Tashev A.N., et al. Discovery of Juniperus sabina var. balkanensis R. P. Adams and A. N. Tashev in Macedonia, Bosnia-Herzegovina, Croatia and Central and Southern Italy and relictual polymorphisms found in nrDNA. Phytologia. 2018;100:117–127.

Chen C., Durand E., Forbes F., François O. Bayesian clustering algorithms ascertaining spatial population structure: A new computer program and a comparison study. Mol. Ecol. Notes. 2007;7:747–756. doi: 10.1111/j.1471-8286.2007.01769.x. DOI

Jakobsson M., Rosenberg N.A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:1801–1806. doi: 10.1093/bioinformatics/btm233. PubMed DOI

Schenk M.F., Thienpont C.-N., Koopman W.J.M., Gilissen L.J.W.J., Smulders M.J.M. Phylogenetic relationships in Betula (Betulaceae) based on AFLP markers. Tree Genet. Genomes. 2008;4:911. doi: 10.1007/s11295-008-0162-0. DOI

Shasany A.K., Darokar M.P., Dhawan S., Gupta A.K., Gupta S., Shukla A.K., Patra N.K., Khanuja S.P.S. Use of RAPD and AFLP markers to identify inter- and intraspecific hybrids of Mentha. J. Hered. 2005;96:542–549. doi: 10.1093/jhered/esi091. PubMed DOI

Divakaran M., Babu K.N., Ravindran P.N., Peter K.V. Interspecific hybridization in Vanilla and molecular characterization of hybrids and selfed progenies using RAPD and AFLP markers. Sci. Hortic. 2006;108:414–422. doi: 10.1016/j.scienta.2006.02.018. DOI

Lazarević M., Siljak-Yakovlev S., Sanino A., Niketić M., Lamy F., Hinsinger D.D., Tomović G., Stevanović B., Stevanović V., Robert T. Genetic variability in Balkan paleoendemic resurrection plants Ramonda serbica and R. nathaliae across their range and in the zone of sympatry. Front. Plant Sci. 2022;13:873471. doi: 10.3389/fpls.2022.873471. PubMed DOI PMC

Douaihy B., Vendramin G.G., Boratyński A., Machon N., Bou Dagher-Kharrat M. High genetic diversity with moderate differentiation in Juniperus excelsa from Lebanon and the Eastern Mediterranean Region. AoB Plants. 2011;2011:plr003. doi: 10.1093/aobpla/plr003. PubMed DOI PMC

Adams R.P., Hojjati F., Schwarzbach A.E. Taxonomy of Juniperus in Iran: DNA sequences of nrDNA plus three cpDNAs reveal Juniperus polycarpos var. turcomanica and J. seravschanica in southern Iran. Phytologia. 2014;96:19–25.

Hojjati F., Kazempour-Osaloo S., Adams R.P., Assadi M. Molecular phylogeny of Juniperus in Iran with special reference to the J. excelsa complex, focusing on J. seravschanica. Phytotaxa. 2018;375:135. doi: 10.11646/phytotaxa.375.2.1. DOI

Elshire R.J., Glaubitz J.C., Sun Q., Poland J.A., Kawamoto K., Buckler E.S., Mitchell S.E. A robust, simple Genotyping-by-Sequencing (GBS) approach for high diversity species. PLoS ONE. 2011;6:e19379. doi: 10.1371/journal.pone.0019379. PubMed DOI PMC

Weitemier K., Straub S.C.K., Cronn R.C., Fishbein M., Schmickl R., McDonnell A., Liston A. Hyb-Seq: Combining target enrichment and genome skimming for plant phylogenomics. Appl. Plant Sci. 2014;2:1400042. doi: 10.3732/apps.1400042. PubMed DOI PMC

Adams R.P. Two new cases of chloroplast capture in incongruent topologies in the Juniperus excelsa complex: J. excelsa var. turcomanica Comb. Nov. and J. excelsa var. seravschanica Comb. Nov. Phytologia. 2016;98:219–231.

Xiong Z., Gaeta R.T., Edger P.P., Cao Y., Zhao K., Zhang S., Pires J.C. Chromosome inheritance and meiotic stability in allopolyploid Brassica napus. G3-Genes Genom Genet. 2021;11:jkaa011. doi: 10.1093/g3journal/jkaa011. PubMed DOI PMC

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